Archives of Pediatric Infectious Diseases

Published by: Kowsar

Genetic Variability and Integron Occurrence in Methicillin Resistant Staphylococcus aureus Strains Recovered from Patients with Urinary Tract Infection

Mehdi Goudarzi 1 , * , Anis Mohammadi 2 , Hossein Goudarzi 1 , Maryam Fazeli 3 and Fattaneh Sabzehali 1
Authors Information
1 Department of Microbiology, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran
2 Department of Biology, North Tehran Branch, Islamic Azad University, Tehran, Iran
3 Department of Virology, Pasteur Institute of Iran, Tehran, Iran
Article information
  • Archives of Pediatric Infectious Diseases: 7 (2); e86189
  • Published Online: April 16, 2019
  • Article Type: Research Article
  • Received: November 8, 2018
  • Revised: January 1, 2019
  • Accepted: January 19, 2019
  • DOI: 10.5812/pedinfect.86189

To Cite: Goudarzi M, Mohammadi A , Goudarzi H , Fazeli M , Sabzehali F . Genetic Variability and Integron Occurrence in Methicillin Resistant Staphylococcus aureus Strains Recovered from Patients with Urinary Tract Infection, Arch Pediatr Infect Dis. Online ahead of Print ; 7(2):e86189. doi: 10.5812/pedinfect.86189.

Copyright © 2019, Author(s). This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International License ( which permits copy and redistribute the material just in noncommercial usages, provided the original work is properly cited.
1. Background
2. Objectives
3. Methods
4. Results
5. Discussion
  • 1. Godaly G, Ambite I, Puthia M, Nadeem A, Ho J, Nagy K, et al. Urinary tract infection molecular mechanisms and clinical translation. Pathogens. 2016;5(1). doi: 10.3390/pathogens5010024. [PubMed: 26927188]. [PubMed Central: PMC4810145].
  • 2. Flores-Mireles AL, Walker JN, Caparon M, Hultgren SJ. Urinary tract infections: Epidemiology, mechanisms of infection and treatment options. Nat Rev Microbiol. 2015;13(5):269-84. doi: 10.1038/nrmicro3432. [PubMed: 25853778]. [PubMed Central: PMC4457377].
  • 3. Muder RR, Brennen C, Rihs JD, Wagener MM, Obman A, Stout JE, et al. Isolation of Staphylococcus aureus from the urinary tract: Association of isolation with symptomatic urinary tract infection and subsequent staphylococcal bacteremia. Clin Infect Dis. 2006;42(1):46-50. doi: 10.1086/498518. [PubMed: 16323090].
  • 4. Baba-Moussa L, Anani L, Scheftel JM, Couturier M, Riegel P, Haikou N, et al. Virulence factors produced by strains of Staphylococcus aureus isolated from urinary tract infections. J Hosp Infect. 2008;68(1):32-8. doi: 10.1016/j.jhin.2007.10.010. [PubMed: 18069084].
  • 5. Chambers HF, Deleo FR. Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat Rev Microbiol. 2009;7(9):629-41. doi: 10.1038/nrmicro2200. [PubMed: 19680247]. [PubMed Central: PMC2871281].
  • 6. Lim WW, Wu P, Bond HS, Wong JY, Ni K, Seto WH, et al. Determinants of methicillin-resistant Staphylococcus aureus (MRSA) prevalence in the Asia-Pacific region: A systematic review and meta-analysis. J Glob Antimicrob Resist. 2019;16:17-27. doi: 10.1016/j.jgar.2018.08.014. [PubMed: 30145271].
  • 7. Boye K, Bartels MD, Andersen IS, Moller JA, Westh H. A new multiplex PCR for easy screening of methicillin-resistant Staphylococcus aureus SCCmec types I-V. Clin Microbiol Infect. 2007;13(7):725-7. doi: 10.1111/j.1469-0691.2007.01720.x. [PubMed: 17403127].
  • 8. Davies J, Davies D. Origins and evolution of antibiotic resistance. Microbiol Mol Biol Rev. 2010;74(3):417-33. doi: 10.1128/MMBR.00016-10. [PubMed: 20805405]. [PubMed Central: PMC2937522].
  • 9. Gillings MR. Integrons: Past, present, and future. Microbiol Mol Biol Rev. 2014;78(2):257-77. doi: 10.1128/MMBR.00056-13. [PubMed: 24847022]. [PubMed Central: PMC4054258].
  • 10. Cambray G, Guerout AM, Mazel D. Integrons. Annu Rev Genet. 2010;44:141-66. doi: 10.1146/annurev-genet-102209-163504. [PubMed: 20707672].
  • 11. Japoni-Nejad A, Rezazadeh M, Kazemian H, Fardmousavi N, van Belkum A, Ghaznavi-Rad E. Molecular characterization of the first community-acquired methicillin-resistant Staphylococcus aureus strains from Central Iran. Int J Infect Dis. 2013;17(11):e949-54. doi: 10.1016/j.ijid.2013.03.023. [PubMed: 23706379].
  • 12. Clinical and Laboratory Standards Institute (CLSI). Performance standards for antimicrobial susceptibility testing; 22th Informational Supplement. CLSI document M100-S22 (ISBN 1-56238-805-3). 2017.
  • 13. Rashidi Nezhad R, Meybodi SM, Rezaee R, Goudarzi M, Fazeli M. Molecular characterization and resistance profile of methicillin resistant staphylococcus aureus strains isolated from hospitalized patients in intensive care unit, Tehran-Iran. Jundishapur J Microbiol. 2017;10(3). doi: 10.5812/jjm.41666.
  • 14. Goudarzi M, Bahramian M, Satarzadeh Tabrizi M, Udo EE, Figueiredo AM, Fazeli M, et al. Genetic diversity of methicillin resistant Staphylococcus aureus strains isolated from burn patients in Iran: ST239-SCCmec III/t037 emerges as the major clone. Microb Pathog. 2017;105:1-7. doi: 10.1016/j.micpath.2017.02.004. [PubMed: 28179118].
  • 15. Hoseini Alfatemi SM, Motamedifar M, Hadi N, Sedigh Ebrahim Saraie H. Analysis of virulence genes among methicillin resistant Staphylococcus aureus (MRSA) strains. Jundishapur J Microbiol. 2014;7(6). e10741. doi: 10.5812/jjm.10741. [PubMed: 25371805]. [PubMed Central: PMC4217665].
  • 16. Ardic N, Sareyyupoglu B, Ozyurt M, Haznedaroglu T, Ilga U. Investigation of aminoglycoside modifying enzyme genes in methicillin-resistant staphylococci. Microbiol Res. 2006;161(1):49-54. doi: 10.1016/j.micres.2005.05.002. [PubMed: 16338590].
  • 17. Martineau F, Picard FJ, Lansac N, Menard C, Roy PH, Ouellette M, et al. Correlation between the resistance genotype determined by multiplex PCR assays and the antibiotic susceptibility patterns of Staphylococcus aureus and Staphylococcus epidermidis. Antimicrob Agents Chemother. 2000;44(2):231-8. doi: 10.1128/AAC.44.2.231-238.2000. [PubMed: 10639342]. [PubMed Central: PMC89663].
  • 18. Udo EE, Jacob LE, Mathew B. Genetic analysis of methicillin-resistant Staphylococcus aureus expressing high- and low-level mupirocin resistance. J Med Microbiol. 2001;50(10):909-15. doi: 10.1099/0022-1317-50-10-909. [PubMed: 11599741].
  • 19. Azimian A, Havaei SA, Fazeli H, Naderi M, Ghazvini K, Samiee SM, et al. Genetic characterization of a vancomycin-resistant Staphylococcus aureus isolate from the respiratory tract of a patient in a university hospital in northeastern Iran. J Clin Microbiol. 2012;50(11):3581-5. doi: 10.1128/JCM.01727-12. [PubMed: 22933598]. [PubMed Central: PMC3486207].
  • 20. Monday SR, Bohach GA. Use of multiplex PCR to detect classical and newly described pyrogenic toxin genes in staphylococcal isolates. J Clin Microbiol. 1999;37(10):3411-4. [PubMed: 10488222]. [PubMed Central: PMC85588].
  • 21. Japoni A, Gudarzi M, Farshad S, Basiri E, Ziyaeyan M, Alborzi A, et al. Assay for integrons and pattern of antibiotic resistance in clinical Escherichia coli strains by PCR-RFLP in Southern Iran. Jpn J Infect Dis. 2008;61(1):85-8. [PubMed: 18219144].
  • 22. Guney AK. A study on class i integrons and antimicrobial resistance among clinical staphylococci isolates from a Turkish hospital. Clin Microbiol. 2014.
  • 23. Aschbacher R, Pichon B, Spoladore G, Pagani E, Innocenti P, Moroder L, et al. High clonal heterogeneity of Panton-Valentine leukocidin-positive meticillin-resistant Staphylococcus aureus strains from skin and soft-tissue infections in the Province of Bolzano, Northern Italy. Int J Antimicrob Agents. 2012;39(6):522-5. doi: 10.1016/j.ijantimicag.2012.02.004. [PubMed: 22481056].
  • 24. Otokunefor K, Sloan T, Kearns AM, James R. Molecular characterization and panton-valentine leucocidin typing of community-acquired methicillin-sensitive Staphylococcus aureus clinical isolates. J Clin Microbiol. 2012;50(9):3069-72. doi: 10.1128/JCM.00602-12. [PubMed: 22718937]. [PubMed Central: PMC3421788].
  • 25. Cirkovic I, Stepanovic S, Skov R, Trajkovic J, Grgurevic A, Larsen AR. Carriage and genetic diversity of methicillin-resistant Staphylococcus aureus among patients and healthcare workers in a Serbian university hospital. PLoS One. 2015;10(5). e0127347. doi: 10.1371/journal.pone.0127347. [PubMed: 25993538]. [PubMed Central: PMC4439055].
  • 26. Wang WY, Chiueh TS, Sun JR, Tsao SM, Lu JJ. Molecular typing and phenotype characterization of methicillin-resistant Staphylococcus aureus isolates from blood in Taiwan. PLoS One. 2012;7(1). e30394. doi: 10.1371/journal.pone.0030394. [PubMed: 22291948]. [PubMed Central: PMC3264593].
  • 27. Lavallee C, Rouleau D, Gaudreau C, Roger M, Tsimiklis C, Locas MC, et al. Performance of an agar dilution method and a Vitek 2 card for detection of inducible clindamycin resistance in Staphylococcus spp. J Clin Microbiol. 2010;48(4):1354-7. doi: 10.1128/JCM.01751-09. [PubMed: 20164285]. [PubMed Central: PMC2849538].
  • 28. Ida T, Okamoto R, Shimauchi C, Okubo T, Kuga A, Inoue M. Identification of aminoglycoside-modifying enzymes by susceptibility testing: Epidemiology of methicillin-resistant Staphylococcus aureus in Japan. J Clin Microbiol. 2001;39(9):3115-21. doi: 10.1128/JCM.39.9.3115-3121.2001. [PubMed: 11526138]. [PubMed Central: PMC88306].
  • 29. Yadegar A, Satri M, Mozafari N. Pervalence ant (4')-Ia gene among nosocomial methicillin resistant Staphylococcus aureus by multiplex-PCR. MJMS. 2010;1:59-68.
  • 30. Imanifooladi AA, Sattari M, Peerayeh SN, Hassan ZM, Hossainidoust SR. Detection the Staphylococcus aureus producing enterotoxin isolated from skin infections in hospitalized patients. Pak J Biol Sci. 2007;10(3):502-5. doi: 10.3923/pjbs.2007.502.505. [PubMed: 19069525].
  • 31. Aydin A, Sudagidan M, Muratoglu K. Prevalence of staphylococcal enterotoxins, toxin genes and genetic-relatedness of foodborne Staphylococcus aureus strains isolated in the Marmara Region of Turkey. Int J Food Microbiol. 2011;148(2):99-106. doi: 10.1016/j.ijfoodmicro.2011.05.007. [PubMed: 21652103].
  • 32. Mashouf RY, Hosseini SM, Mousavi SM, Arabestani MR. Prevalence of enterotoxin genes and antibacterial susceptibility pattern of Staphylococcus aureus strains isolated from animal originated foods in west of Iran. Oman Med J. 2015;30(4):283-90. doi: 10.5001/omj.2015.56. [PubMed: 26366263]. [PubMed Central: PMC4561649].
  • 33. Nowrouzian FL, Dauwalder O, Meugnier H, Bes M, Etienne J, Vandenesch F, et al. Adhesin and superantigen genes and the capacity of Staphylococcus aureus to colonize the infantile gut. J Infect Dis. 2011;204(5):714-21. doi: 10.1093/infdis/jir388. [PubMed: 21844297].
  • 34. Jimenez JN, Ocampo AM, Vanegas JM, Rodriguez EA, Garces CG, Patino LA, et al. Characterisation of virulence genes in methicillin susceptible and resistant Staphylococcus aureus isolates from a paediatric population in a university hospital of Medellin, Colombia. Mem Inst Oswaldo Cruz. 2011;106(8):980-5. doi: 10.1590/S0074-02762011000800013. [PubMed: 22241120].
  • 35. Chen X, Yang HH, Huangfu YC, Wang WK, Liu Y, Ni YX, et al. Molecular epidemiologic analysis of Staphylococcus aureus isolated from four burn centers. Burns. 2012;38(5):738-42. doi: 10.1016/j.burns.2011.12.023. [PubMed: 22360963].
  • 36. Rodrigues MV, Fortaleza CM, Riboli DF, Rocha RS, Rocha C, da Cunha Mde L. Molecular epidemiology of methicillin-resistant Staphylococcus aureus in a burn unit from Brazil. Burns. 2013;39(6):1242-9. doi: 10.1016/j.burns.2013.02.006. [PubMed: 23597850].
  • 37. Perez-Vazquez M, Vindel A, Marcos C, Oteo J, Cuevas O, Trincado P, et al. Spread of invasive Spanish Staphylococcus aureus spa-type t067 associated with a high prevalence of the aminoglycoside-modifying enzyme gene ant(4')-Ia and the efflux pump genes msrA/msrB. J Antimicrob Chemother. 2009;63(1):21-31. doi: 10.1093/jac/dkn430. [PubMed: 18948410].
  • 38. Mostafa M, Siadat SD, Shahcheraghi F, Vaziri F, Japoni-Nejad A, Vand Yousefi J, et al. Variability in gene cassette patterns of class 1 and 2 integrons associated with multi drug resistance patterns in Staphylococcus aureus clinical isolates in Tehran-Iran. BMC Microbiol. 2015;15:152. doi: 10.1186/s12866-015-0488-3. [PubMed: 26228695]. [PubMed Central: PMC4521504].
  • 39. Xu Z, Shi L, Zhang C, Zhang L, Li X, Cao Y, et al. Nosocomial infection caused by class 1 integron-carrying Staphylococcus aureus in a hospital in South China. Clin Microbiol Infect. 2007;13(10):980-4. doi: 10.1111/j.1469-0691.2007.01782.x. [PubMed: 17803751].

Featured Image:

Creative Commons License Except where otherwise noted, this work is licensed under Creative Commons Attribution Non Commercial 4.0 International License .

Search Relations:



Create Citiation Alert
via Google Reader

Readers' Comments